Crayfish Plague and Other Associations
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CHAPTER 30. Parasites and Pathogens: the Crayfish Plague and Other Associations Saprolegniosis (Chapter 29) is a widespread, familiar disease (or a complex of diseases, perhaps) seemingly accorded only a lowly place in the economics of fisheries. Save for occasional outbreaks, it is a malady of endemic proportions with which the freshwater fisheries industries coexist. Not so the crayfish plague (Krebspest, Kräftpesten), caused by Aphanomyces astaci (Schikora, 1906). This is a disease of epidemic extent, and although it affects only a small industry -- the sale and export of edible crayfish, particularly in the Scandinavian Peninsula -- it seriously reduces populations of an animal regarded by many as an irreplaceable delicacy. In this chapter we consider what is known of the crayfish plague, and, as well, chronicle a miscellaneous assortment of case histories of other associations between animals and watermolds. THE CRAYFISH PLAGUE It generally is assumed (Unestam, 1969a) that crayfish plague was first discovered in Italy in 1860 (Seligo, 1895), but perhaps the malady that Ninni referred to in 1865, traced from the Italian province of Lombard, was this disease. In any case, the cause of crayfish disease epidemics was unknown at first. Seligo (1895) published the first extensive account of crayfish plague, noting that the cause had been variously attributed to ectoparasites, bacteria, and even to a vaguely defined “mycosis astacinus.” Although he was not certain that a real connection existed between the annelid worms inhabiting Elodea canadensis Mich. and certain Branchiobdellans (the latter allegedly caused the disease, and were transferred by the annelids), Seligo did not rule out such a possibility. As late as 1934, the supposed relationship between crayfish plague and aquatic vascular plants was being explored. Schiemenz (1934) concluded that these weeds did not really make the aquatic conditions “unhealthy” for crayfish; bacteria were responsible for the disease, he maintained. The first authentic record of crayfish plague in Germany appeared in 1864, where the pestilence evidently had spread from Italy through France. The disease dispersed quickly through Central Europe, reaching Russian waters about 1891 or 1892 (Arnold, 1900), then migrated into Finland in 1893 where it extended its range rapidly throughout the chief crayfish regions (Westman et al., 1973). Subsequently, the plague reached Sweden sometime between 1907 and 1910, and there also became distributed rapidly and widely (Alm, 1929; Vallin, 1932, 1933). In 1900, Mühlen reported a disease outbreak in crayfish in rivers of what is now the southern Estonian and northern Latvian region (formerly USSR). Mannsfield (1942) made an extended study of the plague in this area. The report by Happich (1900) of a “blight” of crayfish may or may not have been of the plague (as it was later to be known). In any case, he believed the cause of the disease he studied was Oidium astaci 433 Happich. Kozłowski (1968) commented on crayfish infection in Polish waters. As of 1969, Vik noted that crayfish plague had not reached Norwegian waters; but in 1972, Håstein and Gladhaug reported finding diseased animals in that country in a river at the Swedish-Norwegian border. Although there seems little doubt that crayfish plague moved through France on its north and eastward spread from Italy, Vey and Vago, in published reports in 1972 and 1973, did not list Aphanomyces astaci as a cause of crayfish disease in France. Vey (1976a, b) did not detect this organism on diseased crayfish in France, and has been unable to authenticate any cases of the plague there (Vey, 1979). THE CAUSAL AGENT Although Hofer had in 1898 ascribed the cause of crayfish plague to Bacillus pestis astaci, it was in 1906 that his chief summary account of the malady appeared. In 1899, A. Weber wrote that Hofer was correct, but Mühlen (1900-01) believed that there were several causes of the disease, among which was a bacterium. By 1903, Schikora had proven to his satisfaction that the plague was caused by a species of Aphanomyces (not then named), and cited experimental supporting evidence from culture work and artificial inoculations. Hofer (1906), in defense of his view that the cause was a bacterium, criticized Schikora for using cultures, because, Hofer maintained, these simply eliminated the organism that was the actual culprit. Prior to Hofer’s account, Hilgendorf (1884) and Leuckart (1884) reviewed the nature of the crayfish disease, and discussed the various hypotheses put forth to explain the cause. It was Schikora, then, who first proposed that crayfish plague was an “aphanomycosis.” He was to repeat this view -- and answer criticisms of it -- in a series of papers culminating in 1926 with an analysis of the previous five decades of work (in part his own) on the disease (Schikora, 1904, 1905, 1906, 1913, 1914, 1922, 1926). Schäperclaus (1927, 1928, 1935) confirmed Schikora’s observations that a species of Aphanomyces was the cause of the disease, chiefly by proving that bacteria were not responsible for the necrosis of crayfish chitin. The very intimate position of the hyphae in and below the chitinous layers of diseased animals was further evidence, he thought, supporting Schikora’s view. Contrary to Schikora’s conclusion that the damaging effect of the fungus was on the invaded animal’s musculature and vital organs, Schäperclaus believed that the Aphanomyces attacked the exoskeleton and nervous system. To Nybelin (1931, 1934, 1936, 1954), working in Sweden, goes the credit for proving through pure culture means that Aphanomyces astaci was the cause of the plague. He isolated the fungus from the ventral nerve cord in the tail of a crayfish after having inoculated the posterior musculature with a small piece of infested cuticle (Nybelin, 1934, 1936). Such inoculations repeatedly resulted in typical symptoms in the test animals within 28-37 days. Nybelin became convinced that A. astaci was in fact specialized for existence in crayfish and unable to survive in nature as a saprophyte (we have collected abundantly in Swedish waters where crayfish plague is known to occur, but have not once recovered the fungus, on baits, in the absence of the host). 434 Rennerfelt (1936) studied extensively the growth of Aphanomyces astaci in culture, giving particular emphasis to the effect of various factors on sporulation and development (Chapters 17, 19). Although he described oogonia and oospores for A. astaci, these have not since been seen, and the illustrations he provided are not convincing. It has been demonstrated on one occasion that genetic strains of Aphanomyces astaci may exist. Unestam and Svensson (1971) experimented with various isolates of the species finding that loss of virulence was reversible (by passage of a virulent strain through a test animal). When a strain no longer was capable of sporulating, however, that loss was permanent. There are several general technical and popular accounts of crayfish plague designed to alert the crayfish-hunting public to the disease and the fungus: Gulbrandsen (1976), Håstein and Unestam (1972), Spitzy (1972), Unestam (1961, 1962, 1964, 1965b, 1968b, 1969a,b, 1970, 1973a, b, 1974b), Wennberg (1963), and Westman (1973). Pauley (1975) regarded the crayfish plague as one of the four most serious infectious diseases of economically important crustaceans. An excellent historical summary of the introduction, use, and economics of the host animal was written (1969a) by Sture Abrahamsson. The series of review accounts and progress reports edited by Fürst (1978) provides especially broad coverage of what is known of the crayfish plague. CHARACTERISTICS OF THE DISEASE Several accounts treat the general symptoms and signs associated with infection in crayfish: Amlacher (1954, 1961, 1970), Benish (1940), Kozowski (1968), Schäperclaus (1935), Tsukeris (1964), and Unestam (1968b), among others. Hyphae of the causal fungus penetrate directly into the chitinous layers, particularly in articulations where the integument is thin. The mycelium grows into the chitin, eventually reaching the musculature and the main elements of the nervous system. In severe cases of infection, filaments may in time grow outward through the chitinous exoskeleton as well. Internally, certain reactions seemingly of a defensive nature appear after the animal is invaded: blood clotting, encapsulation by blood cells, and melanization (Unestam, 1968b, 1974a). There is some evidence (Unestam, 1968b) that exotoxin production damages the nervous system, but according to Benisch (1940), the infected individuals die from bacterial invasion following fungal penetration, or as the result of being unable to molt because of the intramatrical mycelium. These two hypotheses have not gained general acceptance. INOCULATION In view of the persistent spread of the disease geographically, and the rapidity by which Aphanomyces astaci transfers from individual to individual, the fungus must possess a rather efficient mechanism for inoculation. Since A. astaci has no strong 435 chemotactic response -- its planonts are only weakly attracted to crayfish blood (Unestam, 1969d) -- inoculation of susceptible animals in nature would seem chancy at best. The epidemiology of the disease, however, contradicts such a suggestion. The work of Svensson and Unestam (Svensson, 1978) has provided some information on the matter of inoculation. By means of osmotic induction experiments Svensson and Unestam (Svensson, 1978) demonstrated that the